Transient brain-wide coactivations and structured transitions revealed in hemodynamic imaging data

Brain-wide patterns in resting human brains, as either structured functional connectivity (FC) or recurring brain states, have been widely studied in the neuroimaging literature. In particular, resting-state FCs estimated over windowed timeframe neuroimaging data from sub-minutes to minutes using co...

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Main Authors: Ali Fahim Khan, Fan Zhang, Guofa Shou, Han Yuan, Lei Ding
Format: Article
Language:English
Published: Elsevier 2022-10-01
Series:NeuroImage
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811922005766
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author Ali Fahim Khan
Fan Zhang
Guofa Shou
Han Yuan
Lei Ding
author_facet Ali Fahim Khan
Fan Zhang
Guofa Shou
Han Yuan
Lei Ding
author_sort Ali Fahim Khan
collection DOAJ
description Brain-wide patterns in resting human brains, as either structured functional connectivity (FC) or recurring brain states, have been widely studied in the neuroimaging literature. In particular, resting-state FCs estimated over windowed timeframe neuroimaging data from sub-minutes to minutes using correlation or blind source separation techniques have reported many brain-wide patterns of significant behavioral and disease correlates. The present pilot study utilized a novel whole-head cap-based high-density diffuse optical tomography (DOT) technology, together with data-driven analysis methods, to investigate recurring transient brain-wide patterns in spontaneous fluctuations of hemodynamic signals at the resolution of single timeframes from thirteen healthy adults in resting conditions. Our results report that a small number, i.e., six, of brain-wide coactivation patterns (CAPs) describe major spatiotemporal dynamics of spontaneous hemodynamic signals recorded by DOT. These CAPs represent recurring brain states, showing spatial topographies of hemispheric symmetry, and exhibit highly anticorrelated pairs. Moreover, a structured transition pattern among the six brain states is identified, where two CAPs with anterior-posterior spatial patterns are significantly involved in transitions among all brain states. Our results further elucidate two brain states of global positive and negative patterns, indicating transient neuronal coactivations and co-deactivations, respectively, over the entire cortex. We demonstrate that these two brain states are responsible for the generation of a subset of peaks and troughs in global signals (GS), supporting the recent reports on neuronal relevance of hemodynamic GS. Collectively, our results suggest that transient neuronal events (i.e., CAPs), global brain activity, and brain-wide structured transitions co-exist in humans and these phenomena are closely related, which extend the observations of similar neuronal events recently reported in animal hemodynamic data. Future studies on the quantitative relationship among these transient events and their relationships to windowed FCs along with larger sample size are needed to understand their changes with behaviors and diseased conditions.
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spelling doaj.art-d5ffa131ea1f4a1cbcad83b1565614972022-12-22T02:51:11ZengElsevierNeuroImage1095-95722022-10-01260119460Transient brain-wide coactivations and structured transitions revealed in hemodynamic imaging dataAli Fahim Khan0Fan Zhang1Guofa Shou2Han Yuan3Lei Ding4Stephenson School of Biomedical Engineering, University of Oklahoma, 110 W. Boyd St. DEH room 150, Norman, OK 73019, USAStephenson School of Biomedical Engineering, University of Oklahoma, 110 W. Boyd St. DEH room 150, Norman, OK 73019, USAStephenson School of Biomedical Engineering, University of Oklahoma, 110 W. Boyd St. DEH room 150, Norman, OK 73019, USAStephenson School of Biomedical Engineering, University of Oklahoma, 110 W. Boyd St. DEH room 150, Norman, OK 73019, USA; Institute for Biomedical Engineering, Science, and Technology, University of Oklahoma, Norman, USAStephenson School of Biomedical Engineering, University of Oklahoma, 110 W. Boyd St. DEH room 150, Norman, OK 73019, USA; Institute for Biomedical Engineering, Science, and Technology, University of Oklahoma, Norman, USA; Corresponding author at: Stephenson School of Biomedical Engineering, University of Oklahoma, 110 W. Boyd St. DEH room 150, Norman, OK 73019, USA.Brain-wide patterns in resting human brains, as either structured functional connectivity (FC) or recurring brain states, have been widely studied in the neuroimaging literature. In particular, resting-state FCs estimated over windowed timeframe neuroimaging data from sub-minutes to minutes using correlation or blind source separation techniques have reported many brain-wide patterns of significant behavioral and disease correlates. The present pilot study utilized a novel whole-head cap-based high-density diffuse optical tomography (DOT) technology, together with data-driven analysis methods, to investigate recurring transient brain-wide patterns in spontaneous fluctuations of hemodynamic signals at the resolution of single timeframes from thirteen healthy adults in resting conditions. Our results report that a small number, i.e., six, of brain-wide coactivation patterns (CAPs) describe major spatiotemporal dynamics of spontaneous hemodynamic signals recorded by DOT. These CAPs represent recurring brain states, showing spatial topographies of hemispheric symmetry, and exhibit highly anticorrelated pairs. Moreover, a structured transition pattern among the six brain states is identified, where two CAPs with anterior-posterior spatial patterns are significantly involved in transitions among all brain states. Our results further elucidate two brain states of global positive and negative patterns, indicating transient neuronal coactivations and co-deactivations, respectively, over the entire cortex. We demonstrate that these two brain states are responsible for the generation of a subset of peaks and troughs in global signals (GS), supporting the recent reports on neuronal relevance of hemodynamic GS. Collectively, our results suggest that transient neuronal events (i.e., CAPs), global brain activity, and brain-wide structured transitions co-exist in humans and these phenomena are closely related, which extend the observations of similar neuronal events recently reported in animal hemodynamic data. Future studies on the quantitative relationship among these transient events and their relationships to windowed FCs along with larger sample size are needed to understand their changes with behaviors and diseased conditions.http://www.sciencedirect.com/science/article/pii/S1053811922005766Diffuse optical tomographyBrain-wide patternsFunctional connectivityCoactivation patternsGlobal activityTransition
spellingShingle Ali Fahim Khan
Fan Zhang
Guofa Shou
Han Yuan
Lei Ding
Transient brain-wide coactivations and structured transitions revealed in hemodynamic imaging data
NeuroImage
Diffuse optical tomography
Brain-wide patterns
Functional connectivity
Coactivation patterns
Global activity
Transition
title Transient brain-wide coactivations and structured transitions revealed in hemodynamic imaging data
title_full Transient brain-wide coactivations and structured transitions revealed in hemodynamic imaging data
title_fullStr Transient brain-wide coactivations and structured transitions revealed in hemodynamic imaging data
title_full_unstemmed Transient brain-wide coactivations and structured transitions revealed in hemodynamic imaging data
title_short Transient brain-wide coactivations and structured transitions revealed in hemodynamic imaging data
title_sort transient brain wide coactivations and structured transitions revealed in hemodynamic imaging data
topic Diffuse optical tomography
Brain-wide patterns
Functional connectivity
Coactivation patterns
Global activity
Transition
url http://www.sciencedirect.com/science/article/pii/S1053811922005766
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AT guofashou transientbrainwidecoactivationsandstructuredtransitionsrevealedinhemodynamicimagingdata
AT hanyuan transientbrainwidecoactivationsandstructuredtransitionsrevealedinhemodynamicimagingdata
AT leiding transientbrainwidecoactivationsandstructuredtransitionsrevealedinhemodynamicimagingdata